The Structural Basis of Antibody-Antigen Recognition

The function of antibodies (Abs) involves specific binding to antigens (Ags) and activation of other components of the immune system to fight pathogens. The six hypervariable loops within the variable domains of Abs, commonly termed complementarity determining regions (CDRs), are widely assumed to be responsible for Ag recognition, while the constant domains are believed to mediate effector activation. Recent studies and analyses of the growing number of available Ab structures, indicate that this clear functional separation between the two regions may be an oversimplification. Some positions within the CDRs have been shown to never participate in Ag binding and some off-CDRs residues often contribute critically to the interaction with the Ag. Moreover, there is now growing evidence for non-local and even allosteric effects in Ab-Ag interaction in which Ag binding affects the constant region and vice versa. This review summarizes and discusses the structural basis of Ag recognition, elaborating on the contribution of different structural determinants of the Ab to Ag binding and recognition. We discuss the CDRs, the different approaches for their identification and their relationship to the Ag interface. We also review what is currently known about the contribution of non-CDRs regions to Ag recognition, namely the framework regions (FRs) and the constant domains. The suggested mechanisms by which these regions contribute to Ag binding are discussed. On the Ag side of the interaction, we discuss attempts to predict B-cell epitopes and the suggested idea to incorporate Ab information into B-cell epitope prediction schemes. Beyond improving the understanding of immunity, characterization of the functional role of different parts of the Ab molecule may help in Ab engineering, design of CDR-derived peptides, and epitope prediction.

[1]  G. Edelman,et al.  On structural and functional relations between antibodies and proteins of the gamma-system. , 1962, Proceedings of the National Academy of Sciences of the United States of America.

[2]  T. T. Wu,et al.  AN ANALYSIS OF THE SEQUENCES OF THE VARIABLE REGIONS OF BENCE JONES PROTEINS AND MYELOMA LIGHT CHAINS AND THEIR IMPLICATIONS FOR ANTIBODY COMPLEMENTARITY , 1970, The Journal of experimental medicine.

[3]  J. Kehoe,et al.  Variable region sequences of five human immunoglobulin heavy chains of the VH3 subgroup: definitive identification of four heavy chain hypervariable regions. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[4]  S. Cohen,et al.  Antibody structure , 2006 .

[5]  Y. S. Liu,et al.  Primary structure of a human IgA1 immunoglobulin. IV. Streptococcal IgA1 protease, digestion, Fab and Fc fragments, and the complete amino acid sequence of the alpha 1 heavy chain. , 1979, The Journal of biological chemistry.

[6]  K. R. Woods,et al.  Prediction of protein antigenic determinants from amino acid sequences. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Berzofsky,et al.  The antigenic structure of proteins: a reappraisal. , 1984, Annual review of immunology.

[8]  Noncovalent association of heavy and light chains of human immunoglobulins. IV. The roles of the CH1 and CL domains in idiotypic expression. , 1985, Journal of immunology.

[9]  W R Taylor,et al.  Location of ‘continuous’ antigenic determinants in the protruding regions of proteins. , 1986, The EMBO journal.

[10]  G. Rose,et al.  Antigenic determinants in proteins coincide with surface regions accessible to large probes (antibody domains). , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. Poljak,et al.  Three-dimensional structure of an antigen-antibody complex at 2.8 A resolution , 1986, Science.

[12]  P. T. Jones,et al.  Replacing the complementarity-determining regions in a human antibody with those from a mouse , 1986, Nature.

[13]  A. Lesk,et al.  Canonical structures for the hypervariable regions of immunoglobulins. , 1987, Journal of molecular biology.

[14]  C. Milstein,et al.  Reshaping human antibodies: grafting an antilysozyme activity. , 1988, Science.

[15]  J. Blalock,et al.  Inhibition of self-binding antibodies (autobodies) by a VH-derived peptide. , 1988, Science.

[16]  P. T. Jones,et al.  Binding activities of a repertoire of single immunoglobulin variable domains secreted from Escherichia coli , 1989, Nature.

[17]  M Levitt,et al.  A humanized antibody that binds to the interleukin 2 receptor. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A. Lesk,et al.  Conformations of immunoglobulin hypervariable regions , 1989, Nature.

[19]  R. Perlmutter,et al.  Structure and evolution of mammalian VH families. , 1990, International immunology.

[20]  C. Chothia,et al.  The structure of protein-protein recognition sites. , 1990, The Journal of biological chemistry.

[21]  A Tramontano,et al.  Framework residue 71 is a major determinant of the position and conformation of the second hypervariable region in the VH domains of immunoglobulins. , 1990, Journal of molecular biology.

[22]  J Saldanha,et al.  Humanization of a mouse monoclonal antibody by CDR-grafting: the importance of framework residues on loop conformation. , 1991, Protein engineering.

[23]  E. Kabat,et al.  Sequences of proteins of immunological interest , 1991 .

[24]  C. Queen,et al.  Humanized antibodies for therapy , 1991, Nature.

[25]  M Kahn,et al.  Design and synthesis of a mimetic from an antibody complementarity-determining region. , 1991, Science.

[26]  D. Weiner,et al.  Design of bioactive peptides based on antibody hypervariable region structures. Development of conformationally constrained and dimeric peptides with enhanced affinity. , 1991, The Journal of biological chemistry.

[27]  M. Berry,et al.  Use of antibody fragments in immunoaffinity chromatography. Comparison of FV fragments, VH fragments and paralog peptides. , 1992, Journal of chromatography.

[28]  Andrew D. Griffiths,et al.  By–Passing Immunization: Building High Affinity Human Antibodies by Chain Shuffling , 1992, Bio/Technology.

[29]  L. Presta,et al.  Humanization of an anti-p185HER2 antibody for human cancer therapy. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  V. Garsky,et al.  Peptide sequences from the hypervariable regions of two monoclonal anti-idiotypic antibodies against the thyrotropin (TSH) receptor are similar to TSH and inhibit TSH-increased cAMP production in FRTL-5 thyroid cells. , 1992, The Journal of biological chemistry.

[31]  S. Pincus,et al.  Effect of H chain V region on complement activation by immobilized immune complexes. , 1992, Journal of immunology.

[32]  B. Wahrén,et al.  A complementarity-determining region synthetic peptide acts as a miniantibody and neutralizes human immunodeficiency virus type 1 in vitro. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[33]  N. Greenspan,et al.  Role of heavy chain constant domains in antibody-antigen interaction. Apparent specificity differences among streptococcal IgG antibodies expressing identical variable domains. , 1993, Journal of immunology.

[34]  R L Stanfield,et al.  Major antigen-induced domain rearrangements in an antibody. , 1993, Structure.

[35]  E. Lasonder,et al.  Interaction of lysozyme with synthetic anti-lysozyme D1.3 antibody fragments studied by affinity chromatography and surface plasmon resonance. , 1994, Journal of chromatography. A.

[36]  The de novo design of an antibody combining site. Crystallographic analysis of the VL domain confirms the structural model. , 1994, Journal of molecular biology.

[37]  E. Padlan,et al.  Anatomy of the antibody molecule. , 1994, Molecular immunology.

[38]  Chantal Abergel,et al.  Identification of specificity‐determining residues in antibodies , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[39]  T. Clackson,et al.  A hot spot of binding energy in a hormone-receptor interface , 1995, Science.

[40]  R. Mage,et al.  Preferential expansion and survival of B lymphocytes based on VH framework 1 and framework 3 expression: "positive" selection in appendix of normal and VH-mutant rabbits. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[41]  J. Xiang,et al.  Framework residues 71 and 93 of the chimeric B72.3 antibody are major determinants of the conformation of heavy-chain hypervariable loops. , 1995, Journal of molecular biology.

[42]  R. Poljak,et al.  Structural features of the reactions between antibodies and protein antigens , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[43]  Molecular aspects of antibody-antigen interactions: size reduction of a herpes simplex virus neutralizing antibody and its antigen , 1996 .

[44]  M. Buckle,et al.  Can immunoglobulin C(H)1 constant region domain modulate antigen binding affinity of antibodies? , 1996, The Journal of clinical investigation.

[45]  Andrew J. Martin,et al.  Antibody-antigen interactions: contact analysis and binding site topography. , 1996, Journal of molecular biology.

[46]  M. Turner,et al.  Human constant regions influence the antibody binding characteristics of mouse‐human chimeric IgG subclasses , 1996, Immunology.

[47]  C. Borrebaeck,et al.  Light chain shuffling of a high affinity antibody results in a drift in epitope recognition. , 1996, Molecular immunology.

[48]  L. Presta,et al.  Antibody Humanization Using Monovalent Phage Display* , 1997, The Journal of Biological Chemistry.

[49]  S. Jones,et al.  Analysis of protein-protein interaction sites using surface patches. , 1997, Journal of molecular biology.

[50]  A. Lesk,et al.  Standard conformations for the canonical structures of immunoglobulins. , 1997, Journal of molecular biology.

[51]  A. McCoy,et al.  Electrostatic complementarity at protein/protein interfaces. , 1997, Journal of molecular biology.

[52]  S. Jones,et al.  Prediction of protein-protein interaction sites using patch analysis. , 1997, Journal of molecular biology.

[53]  R L Brady,et al.  VL:VH domain rotations in engineered antibodies: Crystal structures of the Fab fragments from two murine antitumor antibodies and their engineered human constructs , 1997, Proteins.

[54]  J. Scardina,et al.  Peptides Derived from the Complementarity-determining Regions of Anti-Mac-1 Antibodies Block Intercellular Adhesion Molecule-1 Interaction with Mac-1* , 1998, The Journal of Biological Chemistry.

[55]  K. Takkinen,et al.  Fine tuning of an anti-testosterone antibody binding site by stepwise optimisation of the CDRs. , 1998, Immunotechnology : an international journal of immunological engineering.

[56]  S. Shapiro,et al.  Cardiolipin binding a light chain from lupus-prone mice. , 1998, Biochemistry.

[57]  Marie-Paule Lefranc,et al.  IMGT, the international ImMunoGeneTics database. , 1997, Nucleic acids research.

[58]  A. Bogan,et al.  Anatomy of hot spots in protein interfaces. , 1998, Journal of molecular biology.

[59]  P. Pothier,et al.  Prophylactic Administration of a Complementarity-Determining Region Derived from a Neutralizing Monoclonal Antibody Is Effective against Respiratory Syncytial Virus Infection in BALB/c Mice , 1998, Journal of Virology.

[60]  B. Sandmaier,et al.  Contributions of a highly conserved VH/VL hydrogen bonding interaction to scFv folding stability and refolding efficiency. , 1998, Biophysical journal.

[61]  M Ohlin,et al.  Complementarity-determining region (CDR) implantation: a theme of recombination. , 1999, Immunotechnology : an international journal of immunological engineering.

[62]  J. Tainer,et al.  Unraveling the effect of changes in conformation and compactness at the antibody VL‐VH interface upon antigen binding , 1999, Journal of molecular recognition : JMR.

[63]  Marie-Paule Lefranc,et al.  IMGT, the international ImMunoGeneTics database , 2001, Nucleic Acids Res..

[64]  T. N. Bhat,et al.  The Protein Data Bank , 2000, Nucleic Acids Res..

[65]  Expression, refolding, and ferritin-binding activity of the isolated VL-domain of monoclonal antibody F11. , 2000, Biochemistry. Biokhimiia.

[66]  Donald M. O'Rourke,et al.  Rationally designed anti-HER2/neu peptide mimetic disables P185HER2/neu tyrosine kinases in vitro and in vivo , 2000, Nature Biotechnology.

[67]  P. Alzari,et al.  Can isotype switch modulate antigen‐binding affinity and influence clonal selection? , 2000, European journal of immunology.

[68]  A. Plückthun,et al.  Yet another numbering scheme for immunoglobulin variable domains: an automatic modeling and analysis tool. , 2001, Journal of molecular biology.

[69]  M. Holmes,et al.  Structural Effects of Framework Mutations on a Humanized Anti-Lysozyme Antibody1 , 2001, The Journal of Immunology.

[70]  L Vidarte,et al.  Serine 132 is the C3 covalent attachment point on the CH1 domain of human IgG1. , 2001, The Journal of biological chemistry.

[71]  Sarah A. Teichmann,et al.  Principles of protein-protein interactions , 2002, ECCB.

[72]  B. Sutton,et al.  Evidence for Involvement of a Hydrophobic Patch in Framework Region 1 of Human V4-34-Encoded Igs in Recognition of the Red Blood Cell I Antigen1 , 2002, The Journal of Immunology.

[73]  A. Casadevall,et al.  Isotype Can Affect the Fine Specificity of an Antibody for a Polysaccharide Antigen1 , 2002, The Journal of Immunology.

[74]  Steven A. Frank,et al.  Immunology and Evolution of Infectious Disease , 2002 .

[75]  K. Tsumoto,et al.  Inhibition of hepatitis C virus NS3 protease by peptides derived from complementarity‐determining regions (CDRs) of the monoclonal antibody 8D4: tolerance of a CDR peptide to conformational changes of a target , 2002, FEBS letters.

[76]  J. Janin,et al.  Dissecting protein–protein recognition sites , 2002, Proteins.

[77]  B. Rost,et al.  Analysing six types of protein-protein interfaces. , 2003, Journal of molecular biology.

[78]  T. Michaelsen,et al.  Binding properties and anti-bacterial activities of V-region identical, human IgG and IgM antibodies, against group B Neisseria meningitidis. , 2003, Biochemical Society transactions.

[79]  V. Giudicelli,et al.  IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. , 2003, Developmental and comparative immunology.

[80]  L. Cavacini,et al.  Expression and functional activity of isotype and subclass switched human monoclonal antibody reactive with the base of the V3 loop of HIV-1 gp120. , 2003, AIDS research and human retroviruses.

[81]  P. Hudson,et al.  Engineered antibodies , 2003, Nature Medicine.

[82]  Masayuki Oda,et al.  Evidence of allosteric conformational changes in the antibody constant region upon antigen binding. , 2003, International immunology.

[83]  Kelvin Hsu,et al.  Molecular signatures of anti-nuclear antibodies--contribution of heavy chain framework residues. , 2003, Molecular immunology.

[84]  Andrew C. R. Martin,et al.  Analysis of the antigen combining site: correlations between length and sequence composition of the hypervariable loops and the nature of the antigen. , 2003, Journal of molecular biology.

[85]  Mayuko Takeda-Shitaka,et al.  Interaction between the antigen and antibody is controlled by the constant domains: Normal mode dynamics of the HEL–HyHEL‐10 complex , 2003, Protein science : a publication of the Protein Society.

[86]  R. Nussinov,et al.  Protein–protein interactions: Structurally conserved residues distinguish between binding sites and exposed protein surfaces , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[87]  Vladimir Brusic,et al.  Computational methods for prediction of T-cell epitopes--a framework for modelling, testing, and applications. , 2004, Methods.

[88]  Mats Ohlin,et al.  Length of the antibody heavy chain complementarity determining region 3 as a specificity‐determining factor , 2004, Journal of molecular recognition : JMR.

[89]  G. Denardo,et al.  A review of human anti-globulin antibody (HAGA, HAMA, HACA, HAHA) responses to monoclonal antibodies. Not four letter words. , 2004, The quarterly journal of nuclear medicine and molecular imaging : official publication of the Italian Association of Nuclear Medicine (AIMN) [and] the International Association of Radiopharmacology (IAR), [and] Section of the Society of....

[90]  R. Raz,et al.  ProMate: a structure based prediction program to identify the location of protein-protein binding sites. , 2004, Journal of molecular biology.

[91]  Yan Li,et al.  Rational design of potent mimic peptide derived from monoclonal antibody: antibody mimic design. , 2005, Immunology letters.

[92]  D. Flower,et al.  Benchmarking B cell epitope prediction: Underperformance of existing methods , 2005, Protein science : a publication of the Protein Society.

[93]  A. Casadevall,et al.  Variable-Region-Identical Antibodies Differing in Isotype Demonstrate Differences in Fine Specificity and Idiotype1 , 2005, The Journal of Immunology.

[94]  Fred Dyda,et al.  Water molecules in the antibody-antigen interface of the structure of the Fab HyHEL-5-lysozyme complex at 1.7 A resolution: comparison with results from isothermal titration calorimetry. , 2005, Acta crystallographica. Section D, Biological crystallography.

[95]  P. Hudson,et al.  Engineered antibody fragments and the rise of single domains , 2005, Nature Biotechnology.

[96]  Ruben Abagyan,et al.  Statistical analysis and prediction of protein–protein interfaces , 2005, Proteins.

[97]  Urmila Kulkarni-Kale,et al.  CEP: a conformational epitope prediction server , 2005, Nucleic Acids Res..

[98]  I. Roterman,et al.  The Indirect Generation of Long‐distance Structural Changes in Antibodies upon their Binding to Antigen , 2006, Chemical biology & drug design.

[99]  M. Kojima,et al.  The role of interface framework residues in determining antibody VH/VL interaction strength and antigen‐binding affinity , 2006, The FEBS journal.

[100]  S. Crotty,et al.  Immunity and immunological memory following smallpox vaccination , 2006, Immunological reviews.

[101]  Ozlem Keskin,et al.  Binding induced conformational changes of proteins correlate with their intrinsic fluctuations: a case study of antibodies , 2007, BMC Structural Biology.

[102]  J. Salfeld,et al.  Isotype selection in antibody engineering , 2007, Nature Biotechnology.

[103]  P. Bourne,et al.  Antibody-protein interactions: benchmark datasets and prediction tools evaluation , 2007 .

[104]  C. MacKenzie,et al.  Isolation and affinity maturation of hapten-specific antibodies. , 2007, Biotechnology advances.

[105]  Avner Schlessinger,et al.  Towards a consensus on datasets and evaluation metrics for developing B‐cell epitope prediction tools , 2007, Journal of molecular recognition : JMR.

[106]  A. Casadevall,et al.  The Immunoglobulin Heavy Chain Constant Region Affects Kinetic and Thermodynamic Parameters of Antibody Variable Region Interactions with Antigen* , 2007, Journal of Biological Chemistry.

[107]  S. Batra,et al.  Engineering antibodies for clinical applications. , 2007, Trends in biotechnology.

[108]  Wei Wang,et al.  Antibody structure, instability, and formulation. , 2007, Journal of pharmaceutical sciences.

[109]  Wei Li,et al.  ElliPro: a new structure-based tool for the prediction of antibody epitopes , 2008, BMC Bioinformatics.

[110]  Kouhei Tsumoto,et al.  Critical contribution of VH–VL interaction to reshaping of an antibody: The case of humanization of anti‐lysozyme antibody, HyHEL‐10 , 2008, Protein science : a publication of the Protein Society.

[111]  Haruki Nakamura,et al.  Structural classification of CDR‐H3 revisited: A lesson in antibody modeling , 2008, Proteins.

[112]  M. Juliano,et al.  Antibody Complementarity-Determining Regions (CDRs) Can Display Differential Antimicrobial, Antiviral and Antitumor Activities , 2008, PloS one.

[113]  A. Casadevall,et al.  The immunoglobulin constant region contributes to affinity and specificity. , 2008, Trends in immunology.

[114]  B. Rost,et al.  Automated Identification of Complementarity Determining Regions (CDRs) Reveals Peculiar Characteristics of CDRs and B Cell Epitopes1 , 2008, The Journal of Immunology.

[115]  A. Casadevall,et al.  Isothermal Titration Calorimetry Reveals Differential Binding Thermodynamics of Variable Region-identical Antibodies Differing in Constant Region for a Univalent Ligand* , 2008, Journal of Biological Chemistry.

[116]  Pierre Baldi,et al.  PEPITO: improved discontinuous B-cell epitope prediction using multiple distance thresholds and half sphere exposure , 2008, Bioinform..

[117]  A. Stringaro,et al.  Protection by Anti-β-Glucan Antibodies Is Associated with Restricted β-1,3 Glucan Binding Specificity and Inhibition of Fungal Growth and Adherence , 2009, PloS one.

[118]  Chi Zhang,et al.  Prediction of antigenic epitopes on protein surfaces by consensus scoring , 2009, BMC Bioinformatics.

[119]  Xinglong Yu,et al.  An introduction to epitope prediction methods and software , 2009, Reviews in medical virology.

[120]  Di Wu,et al.  SEPPA: a computational server for spatial epitope prediction of protein antigens , 2009, Nucleic Acids Res..

[121]  Nimrod D. Rubinstein,et al.  A machine-learning approach for predicting B-cell epitopes. , 2009, Molecular immunology.

[122]  Itay Mayrose,et al.  Epitopia: a web-server for predicting B-cell epitopes , 2009, BMC Bioinformatics.

[123]  Janice M Reichert,et al.  Development trends for therapeutic antibody fragments , 2009, Nature Biotechnology.

[124]  Yanay Ofran Prediction of Protein Interaction Sites , 2009 .

[125]  Jinyan Li,et al.  Mining for the antibody-antigen interacting associations that predict the B cell epitopes , 2010, BMC Structural Biology.

[126]  Gajendra PS Raghava,et al.  Identification of conformational B-cell Epitopes in an antigen from its primary sequence , 2010, Immunome research.

[127]  Hiroki Shirai,et al.  Use of amino acid composition to predict epitope residues of individual antibodies. , 2010, Protein engineering, design & selection : PEDS.

[128]  Di Wu,et al.  Evaluation of spatial epitope computational tools based on experimentally-confirmed dataset for protein antigens , 2010 .

[129]  Bo Yao,et al.  EPSVR and EPMeta: prediction of antigenic epitopes using support vector regression and multiple server results , 2010, BMC Bioinformatics.

[130]  A. Casadevall,et al.  Circular Dichroism reveals evidence of coupling between immunoglobulin constant and variable region secondary structure. , 2010, Molecular immunology.

[131]  S. Pillai,et al.  B cells and autoimmunity. , 2011, Current opinion in immunology.

[132]  Bjoern Peters,et al.  Applications for T-cell epitope queries and tools in the Immune Epitope Database and Analysis Resource. , 2011, Journal of immunological methods.

[133]  Benoit M. Macq,et al.  Identification of Relevant Properties for Epitopes Detection Using a Regression Model , 2011, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[134]  Min-Yuan Chou,et al.  Humanization and Characterization of an Anti-Human TNF-α Murine Monoclonal Antibody , 2011, PloS one.

[135]  Jinyan Li,et al.  Antibody-Specified B-Cell Epitope Prediction in Line with the Principle of Context-Awareness , 2011, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[136]  Meng Zhao,et al.  Prediction of conformational B-cell epitopes from 3D structures by random forests with a distance-based feature , 2011, BMC Bioinformatics.

[137]  Yanay Ofran,et al.  A Systematic Comparison of Free and Bound Antibodies Reveals Binding-Related Conformational Changes , 2012, The Journal of Immunology.

[138]  Yanay Ofran,et al.  Paratome: an online tool for systematic identification of antigen-binding regions in antibodies based on sequence or structure , 2012, Nucleic Acids Res..

[139]  M. Zurini,et al.  Current strategies in antibody engineering: Fc engineering and pH-dependent antigen binding, bispecific antibodies and antibody drug conjugates. , 2012, Biotechnology journal.

[140]  A. Casadevall,et al.  Immunoglobulin isotype influences affinity and specificity , 2012, Proceedings of the National Academy of Sciences.

[141]  A. Casadevall,et al.  The constant region contributes to the antigenic specificity and renal pathogenicity of murine anti-DNA antibodies. , 2012, Journal of autoimmunity.

[142]  G. Raghunathan,et al.  Antigen‐binding site anatomy and somatic mutations in antibodies that recognize different types of antigens , 2012, Journal of molecular recognition : JMR.

[143]  L. Lopalco,et al.  Isotype modulates epitope specificity, affinity, and antiviral activities of anti–HIV-1 human broadly neutralizing 2F5 antibody , 2012, Proceedings of the National Academy of Sciences.

[144]  J. Haidar,et al.  A universal combinatorial design of antibody framework to graft distinct CDR sequences: A bioinformatics approach , 2012, Proteins.

[145]  L. Possani,et al.  A single mutation in framework 2 of the heavy variable domain improves the properties of a diabody and a related single-chain antibody. , 2012, Journal of molecular biology.

[146]  Yanay Ofran,et al.  Structural Consensus among Antibodies Defines the Antigen Binding Site , 2012, PLoS Comput. Biol..

[147]  Peter G. Schultz,et al.  Reshaping Antibody Diversity , 2013, Cell.

[148]  Y. Ofran,et al.  The indistinguishability of epitopes from protein surface is explained by the distinct binding preferences of each of the six antigen-binding loops. , 2013, Protein engineering, design & selection : PEDS.

[149]  A. Casadevall,et al.  The constant region affects antigen binding of antibodies to DNA by altering secondary structure. , 2013, Molecular immunology.

[150]  Søren B. Padkjær,et al.  Structural analysis of B-cell epitopes in antibody:protein complexes. , 2013, Molecular immunology.

[151]  Herman W T van Vlijmen,et al.  Antibody humanization by redesign of complementarity-determining region residues proximate to the acceptor framework. , 2014, Methods.